Valproate reduces tau phosphorylation via cyclin-dependent kinase 5 and glycogen synthase kinase 3 signaling pathways

Brain Research Bulletin

Volumn 85, Issue 3-4, 2011, Pages 194-200

  Hu, Jiang Ping ^a,b   Xie, Jing Wei ^a   Wang, Chun Yan ^a   Wang, Tao ^a   Wang, Xu ^a   Wang, Si Ling ^c   Teng, Wei Ping ^a   Wang, Zhan You ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b MUDANJIANG MEDICAL UNIVERSITY   (China)

^c SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; APP PS1 transgenic mouse; CDK5; GSK3; Okadaic acid; Tau; Valproate

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3; OKADAIC ACID; PRESENILIN; SERINE; TAU PROTEIN; THREONINE; VALPROIC ACID;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYSTEMIC THERAPY; TRANSGENIC MOUSE;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CALPAIN; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE 5; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICE; MICE, TRANSGENIC; NEUROBLASTOMA; PHOSPHORYLATION; PRESENILIN-1; SIGNAL TRANSDUCTION; TAU PROTEINS; THREONINE; VALPROIC ACID;

EID: 79957852572     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2011.03.006     Document Type: Article

References (52)

1. Alonso A.C., Grundke-Iqbal I., Iqbal K. Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat. Med. 1996, 2:783-787.
2. Alvarez A., Munoz J.P., Maccioni R.B. A Cdk5-p35 stable complex is involved in the beta-amyloid-induced deregulation of Cdk5 activity in hippocampal neurons. Exp. Cell Res. 2001, 264:266-274.
3. Ballatore C., Lee V.M., Trojanowski J.Q. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat. Rev. Neurosci. 2007, 8:663-672.
4. Blennow K., de Leon M.J., Zetterberg H. Alzheimer's disease. Lancet 2006, 368:387-403.
5. Cancino G.I., Perez de Arce K., Castro P.U., Toledo E.M., von Bernhardi R., Alvarez A.R. c-Abl tyrosine kinase modulates tau pathology and Cdk5 phosphorylation in AD transgenic mice. Neurobiol. Aging 2009, 10.1016/j.neurobiolaging.2009.07.007.
6. Chen P.S., Peng G.S., Li G., Yang S., Wu X., Wang C.C., Wilson B., Lu R.B., Gean P.W., Chuang D.M., Hong J.S. Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry 2006, 11:1116-1125.
7. Czuczwar S.J., Patsalos P.N. The new generation of GABA enhancers. Potential in the treatment of epilepsy. CNS Drugs 2001, 15:339-350.
8. Dajani R., Fraser E., Roe S.M., Young N., Good V., Dale T.C., Pearl L.H. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 2001, 105:721-732.
9. Ding Y., Qiao A., Wang Z., Goodwin J.S., Lee E.S., Block M.L., Allsbrook M., McDonald M.P., Fan G.H. Retinoic acid attenuates beta-amyloid deposition and rescues memory deficits in an Alzheimer's disease transgenic mouse model. J. Neurosci. 2008, 28:11622-11634.
10. Dou H., Birusingh K., Faraci J., Gorantla S., Poluektova L.Y., Maggirwar S.B., Dewhurst S., Gelbard H.A., Gendelman H.E. Neuroprotective activities of sodium valproate in a murine model of human immunodeficiency virus-1 encephalitis. J. Neurosci. 2003, 23:9162-9170.
11. Ekinci F.J., Ortiz D., Shea T.B. Okadaic acid mediates tau phosphorylation via sustained activation of the L-voltage-sensitive calcium channel. Brain Res. Mol. Brain Res. 2003, 117:145-151.
12. Engmann O., Giese K.P. Crosstalk between Cdk5 and GSK3beta: implications for Alzheimer's disease. Front. Mol. Neurosci. 2009, 2:2.
13. Giese K.P. GSK-3: a key player in neurodegeneration and memory. IUBMB Life 2009, 61:516-521.
14. Gong C.X., Liu F., Grundke-Iqbal I., Iqbal K. Post-translational modifications of tau protein in Alzheimer's disease. J. Neural Transm. 2005, 112:813-838.
15. Grundke-Iqbal I., Rolkova G., Konstekova E., Iqbal K. Biological markers in Alzheimer's disease. Bratisl. Lek. Listy 2006, 107:359-365.
16. Hanger D.P., Betts J.C., Loviny T.L., Blackstock W.P., Anderton B.H. New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry. J. Neurochem. 1998, 71:2465-2476.
17. Hoe H.S., Freeman J., Rebeck G.W. Apolipoprotein E decreases tau kinases and phospho-tau levels in primary neurons. Mol. Neurodegener. 2006, 1:18.
18. Hooper C., Killick R., Lovestone S. The GSK3 hypothesis of Alzheimer's disease. J. Neurochem. 2008, 104:1433-1439.
19. Hughes K., Nikolakaki E., Plyte S.E., Totty N.F., Woodgett J.R. Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 1993, 12:803-808.
20. Imahori K., Uchida T. Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J. Biochem. 1997, 121:179-188.
21. Iqbal K., Alonso Adel C., Chen S., Chohan M.O., El-Akkad E., Gong C.X., Khatoon S., Li B., Liu F., Rahman A., Tanimukai H., Grundke-Iqbal I. Tau pathology in Alzheimer disease and other tauopathies. Biochim. Biophys. Acta 2005, 1739:198-210.
22. Iqbal K., Grundke-Iqbal I. Discoveries of tau, abnormally hyperphosphorylated tau and others of neurofibrillary degeneration: a personal historical perspective. J. Alzheimers Dis. 2006, 9:219-242.
23. Kitazawa M., Cheng D., Laferla F.M. Chronic copper exposure exacerbates both amyloid and tau pathology and selectively dysregulates cdk5 in a mouse model of AD. J. Neurochem. 2009, 108:1550-1560.
24. Lee M.S., Tsai L.H. Cdk5: one of the links between senile plaques and neurofibrillary tangles?. J. Alzheimers Dis. 2003, 5:127-137.
25. Liu F., Liang Z., Shi J., Yin D., El-Akkad E., Grundke-Iqbal I., Iqbal K., Gong C.X. PKA modulates GSK-3beta- and cdk5-catalyzed phosphorylation of tau in site- and kinase-specific manners. FEBS Lett. 2006, 580:6269-6274.
26. Lovestone S., Reynolds C.H. The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 1997, 78:309-324.
27. Mazanetz M.P., Fischer P.M. Untangling tau hyperphosphorylation in drug design for neurodegenerative diseases. Nat. Rev. Drug Discov. 2007, 6:464-479.
28. Minegishi S., Asada A., Miyauchi S., Fuchigami T., Saito T., Hisanaga S. Membrane association facilitates degradation and cleavage of the cyclin-dependent kinase 5 activators p35 and p39. Biochemistry 2010, 49:5482-5493.
29. Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Yoshida H., Titani K., Ihara Y. Proline-directed and non-proline-directed phosphorylation of PHF-tau. J. Biol. Chem. 1995, 270:823-829.
30. Patrick G.N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P., Tsai L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999, 402:615-622.
31. Pei J.J., Tanaka T., Tung Y.C., Braak E., Iqbal K., Grundke-Iqbal I. Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J. Neuropathol. Exp. Neurol. 1997, 56:70-78.
32. Plant K.E., Anderson E., Simecek N., Brown R., Forster S., Spinks J., Toms N., Gibson G.G., Lyon J., Plant N. The neuroprotective action of the mood stabilizing drugs lithium chloride and sodium valproate is mediated through the up-regulation of the homeodomain protein Six1. Toxicol. Appl. Pharmacol. 2009, 235:124-134.
33. Qing H., He G., Ly P.T., Fox C.J., Staufenbiel M., Cai F., Zhang Z., Wei S., Sun X., Chen C.H., Zhou W., Wang K., Song W. Valproic acid inhibits Abeta production, neuritic plaque formation, and behavioral deficits in Alzheimer's disease mouse models. J. Exp. Med. 2008, 205:2781-2789.
34. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 2001, 81:741-766.
35. Sereno L., Coma M., Rodriguez M., Sanchez-Ferrer P., Sanchez M.B., Gich I., Agullo J.M., Perez M., Avila J., Guardia-Laguarta C., Clarimon J., Lleo A., Gomez-Isla T. A novel GSK-3beta inhibitor reduces Alzheimer's pathology and rescues neuronal loss in vivo. Neurobiol. Dis. 2009, 35:359-367.
36. Shelton S.B., Krishnamurthy P., Johnson G.V. Effects of cyclin-dependent kinase-5 activity on apoptosis and tau phosphorylation in immortalized mouse brain cortical cells. J. Neurosci. Res. 2004, 76:110-120.
37. Shi H.R., Zhu L.Q., Wang S.H., Liu X.A., Tian Q., Zhang Q., Wang Q., Wang J.Z. 17beta-estradiol attenuates glycogen synthase kinase-3beta activation and tau hyperphosphorylation in Akt-independent manner. J. Neural Transm. 2008, 115:879-888.
38. Stambolic V., Woodgett J.R. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem. J. 1994, 303:701-704. (Pt 3).
39. Su Y., Ryder J., Li B., Wu X., Fox N., Solenberg P., Brune K., Paul S., Zhou Y., Liu F., Ni B. Lithium, a common drug for bipolar disorder treatment, regulates amyloid-beta precursor protein processing. Biochemistry 2004, 43:6899-6908.
40. Takashima A., Murayama M., Yasutake K., Takahashi H., Yokoyama M., Ishiguro K. Involvement of cyclin dependent kinase5 activator p25 on tau phosphorylation in mouse brain. Neurosci. Lett. 2001, 306:37-40.
41. Tariot P.N., Aisen P.S. Can lithium or valproate untie tangles in Alzheimer's disease?. J. Clin. Psychiatry 2009, 70:919-921.
42. Tsai L.H., Lee M.S., Cruz J. Cdk5, a therapeutic target for Alzheimer's disease?. Biochim. Biophys. Acta 2004, 1697:137-142.
43. Tseng H.C., Zhou Y., Shen Y., Tsai L.H. A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett. 2002, 523:58-62.
44. Voss K., Gamblin T.C. GSK-3beta phosphorylation of functionally distinct tau isoforms has differential, but mild effects. Mol. Neurodegener. 2009, 4:18.
45. Wang X., Zheng W., Xie J.W., Wang T., Wang S.L., Teng W.P., Wang Z.Y. Insulin deficiency exacerbates cerebral amyloidosis and behavioral deficits in an Alzheimer transgenic mouse model. Mol. Neurodegener. 2010, 5:46.
46. Williams R.S., Cheng L., Mudge A.W., Harwood A.J. A common mechanism of action for three mood-stabilizing drugs. Nature 2002, 417:292-295.
47. Yu S., Zheng W., Xin N., Chi Z.H., Wang N.Q., Nie Y.X., Feng W.Y., Wang Z.Y. Curcumin prevents dopaminergic neuronal death through inhibition of the c-Jun N-terminal kinase pathway. Rejuvenation Res. 2010, 13:55-64.
48. Yuan P.X., Huang L.D., Jiang Y.M., Gutkind J.S., Manji H.K., Chen G. The mood stabilizer valproic acid activates mitogen-activated protein kinases and promotes neurite growth. J. Biol. Chem. 2001, 276:31674-31683.
49. Zhang L.H., Wang X., Zheng Z.H., Ren H., Stoltenberg M., Danscher G., Huang L., Rong M., Wang Z.Y. Altered expression and distribution of zinc transporters in APP/PS1 transgenic mouse brain. Neurobiol. Aging 2010, 31:74-87.
50. Zhang Z., Simpkins J.W. An okadaic acid-induced model of tauopathy and cognitive deficiency. Brain Res. 2010, 1359:233-246.
51. Zhang Z., Simpkins J.W. Okadaic acid induces tau phosphorylation in SH-SY5Y cells in an estrogen-preventable manner. Brain Res. 2010, 176-181.
52. Zheng Y.L., Kesavapany S., Gravell M., Hamilton R.S., Schubert M., Amin N., Albers W., Grant P., Pant H.C. A Cdk5 inhibitory peptide reduces tau hyperphosphorylation and apoptosis in neurons. EMBO J. 2005, 24:209-220.